Dichotomy in the evolution of pathogenicity island and bacteriophage encoded integrases from pathogenic Escherichia coli strains

Infection, Genetics and Evolution

Volumn 11, Issue 2, 2011, Pages 423-436

  Napolitano, Michael G ^a   Almagro Moreno, Salvador ^a,b   Boyd, E Fidelma ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Escherichia coli evolution; Pathogenicity islands; Prophages

Indexed keywords

INTEGRASE; RECOMBINASE; TRANSFER RNA; TYROSINE RECOMBINASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIOPHAGE; CHROMOSOME; DNA BASE COMPOSITION; DNA STRUCTURE; ESCHERICHIA COLI; GENE SEQUENCE; GENETIC RECOMBINATION; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY ISLAND; PHYLOGENY; PRIORITY JOURNAL;

BASE COMPOSITION; BASE SEQUENCE; COLIPHAGES; CONSERVED SEQUENCE; DNA, BACTERIAL; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GENOMIC ISLANDS; INTEGRASES; INTERSPERSED REPETITIVE SEQUENCES; PHYLOGENY; RECOMBINATION, GENETIC; RNA, TRANSFER; SEQUENCE ALIGNMENT; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 79951954582     PISSN: 15671348     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meegid.2010.12.003     Document Type: Article

References (96)

1. Afset J., Anderssen E., Bruant G., Harel J., Wieler L., Bergh K. Phylogenetic backgrounds and virulence profiles of atypical enteropathogenic Escherichia coli strains from a case-control study using multilocus sequence typing and DNA microarray analysis. J. Clin. Microbiol. 2008, 46:2280-2290.
2. Almagro-Moreno S., Napolitano M.G., Boyd E.F. Excision dynamics of Vibrio pathogenicity island-2 from Vibrio cholerae: role of a recombination directionality factor VefA. BMC Microbiol. 2010, 10:306.
3. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
4. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
5. Beaber J., Hochhut B., Waldor M. Genomic and functional analyses of SXT, an integrating antibiotic resistance gene transfer element derived from Vibrio cholerae. J. Bacteriol. 2002, 184:4259-4269.
6. Blattner F.R., Plunkett G., Bloch C.A., et al. The complete genome sequence of Escherichia coli K-12. Science 1997, 277:1453-1474.
7. Blum G., Ott M., Lischewski A., Ritter A., Imrich H., Tschape H., Hacker J. Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of an Escherichia coli wild-type pathogen. Infect. Immun. 1994, 62:606-614.
8. Böltner D., MacMahon C., Pembroke J., Strike P., Osborn A. R391: a conjugative integrating mosaic comprised of phage, plasmid, and transposon elements. J. Bacteriol. 2002, 184:5158-5169.
9. Boyd E.F., Hartl D.L. Chromosomal regions specific to pathogenic isolates of Escherichia coli have a phylogenetically clustered distribution. J. Bacteriol. 1998, 180:1159-1165.
10. Boyd E.F., Brussow H. Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol. 2002, 10:521-529.
11. Boyd E.F., Almagro-Moreno S., Parent M.A. Genomic islands are dynamic, ancient integrative elements in bacterial evolution. Trends Microbiol. 2009, 17:47-53.
12. Briani F., Deho G., Forti F., Ghisotti D. The plasmid status of satellite bacteriophage P4. Plasmid 2001, 45:1-17.
13. Brussow H., Canchaya C., Hardt W.D. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 2004, 68:560-602.
14. Buchrieser C., Prentice M., Carniel E. The 102-kilobase unstable region of Yersinia pestis comprises a high-pathogenicity island linked to a pigmentation segment which undergoes internal rearrangement. J. Bacteriol. 1998, 180:2321-2329.
15. Burrus V., Pavlovic G., Decaris B., Guedon G. Conjugative transposons: the tip of the iceberg. Mol. Microbiol. 2002, 46:601-610.
16. Burrus V., Waldor M.K. Control of SXT integration and excision. J. Bacteriol. 2003, 185:5045-5054.
17. Burrus V., Marrero J., Waldor M.K. The current ICE age: biology and evolution of SXT-related integrating conjugative elements. Plasmid 2006, 55:173-183.
18. Casjens S., Winn-Stapley D.A., Gilcrease E.B., Morona R., Kuhlewein C., Chua J.E., Manning P.A., Inwood W., Clark A.J. The chromosome of Shigella flexneri bacteriophage Sf6: complete nucleotide sequence, genetic mosaicism, and DNA packaging. J. Mol. Biol. 2004, 339:379-394.
19. Dobrindt U., Blum-Oehler G., Nagy G., Schneider G., Johann A., Gottschalk G., Hacker J. Genetic structure and distribution of four pathogenicity islands (PAI I(536) to PAI IV(536)) of uropathogenic Escherichia coli strain 536. Infect. Immun. 2002, 70:6365-6372.
20. Dobrindt U., Hochhut B., Hentschel U., Hacker J. Genomic islands in pathogenic and environmental microorganisms. Nat. Rev. Microbiol. 2004, 2:414-424.
21. Dobrindt U., Chowdary M., Krumbholz G., Hacker J. Genome dynamics and its impact on evolution of Escherichia coli. Med. Microbiol. Immunol. 2010, 199:145-154.
22. Dobrindt U., Chowdary M.G., Krumbholz G., Hacker J. Genome dynamics and its impact on evolution of Escherichia coli. Med. Microbiol. Immunol. 2010, (Epub ahead of print).
23. Dziejman M., Balon E., Boyd D., Fraser C.M., Heidelberg J.F., Mekalanos J.J. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:1556-1561.
24. Edgar R. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 5:1792-1797.
25. Esposito D., Scocca J. The integrase family of tyrosine recombinases: evolution of a conserved active site domain. Nucleic Acids Res. 1997, 25:3605-3614.
26. Feng P., Keys C., Lacher D., Monday S., Shelton D., Rozand C., Rivas M., Whittam T. Prevalence, characterization and clonal analysis of Escherichia coli O157: non-H7 serotypes that carry eae alleles. FEMS Microbiol. Lett. 2010, 308:62-67.
27. Frost L.S., Leplae R., Summers A.O., Toussaint A. Mobile genetic elements: the agents of open source evolution. Nat. Rev. Microbiol. 2005, 3:722-732.
28. Gemski P., Koeltzow D.E., Formal S.B. Phage conversion of Shigella flexneri group antigens. Infect. Immun. 1975, 11:685-691.
29. Gordon D., Clermont O., Tolley H., Denamur E. Assigning Escherichia coli strains to phylogenetic groups: multi-locus sequence typing versus the PCR triplex method. Environ. Microbiol. 2008, 10:2484-2496.
30. Groisman E., Ochman H. Pathogenicity islands: bacterial evolution in quantum leaps. Cell 1996, 87:791-794.
31. Hacker J., Blum-Oehler G., Muhldorfer I., Tschape H. Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol. Microbiol. 1997, 23:1089-1097.
32. Hacker J., Carniel E. Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. EMBO Rep. 2001, 2:376-381.
33. Hayashi T., Makino K., Ohnishi M., et al. Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res. 2001, 8:11-22.
34. He J., Baldini R.L., Deziel E., et al. The broad host range pathogen Pseudomonas aeruginosa strain PA14 carries two pathogenicity islands harboring plant and animal virulence genes. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:2530-2535.
35. Hochhut B., Waldor M.K. Site-specific integration of the conjugal Vibrio cholerae SXT element into prfC. Mol. Microbiol. 1999, 32:99-110.
36. Hochhut B., Wilde C., Balling G., Middendorf B., Dobrindt U., Brzuszkiewicz E., Gottschalk G., Carniel E., Hacker J. Role of pathogenicity island-associated integrases in the genome plasticity of uropathogenic Escherichia coli strain 536. Mol. Microbiol. 2006, 61:584-595.
37. Hurley C.C., Quirke A., Reen F.J., Boyd E.F. Four genomic islands that mark post-1995 pandemic Vibrio parahaemolyticus isolates. BMC Genomics 2006, 7:104.
38. Jaureguy F., Landraud L., Passet V., et al. Phylogenetic and genomic diversity of human bacteremic Escherichia coli strains. BMC Genomics 2008, 9:560.
39. Jermyn W.S., Boyd E.F. Characterization of a novel Vibrio pathogenicity island (VPI-2) encoding neuraminidase (nanH) among toxigenic Vibrio cholerae isolates. Microbiology 2002, 148:3681-3693.
40. Johnson J., Johnston B., Clabots C.R., Kuskowski M.A., Roberts E., DebRoy C. Virulence genotypes and phylogenetic background of Escherichia coli serogroup O6 isolates from humans, dogs, and cats. J. Clin. Microbiol. 2008, 46:417-422.
41. Johnson T.J., Kariyawasam S., Wannemuehler Y., et al. The genome sequence of avian pathogenic Escherichia coli strain O1:K1:H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. J. Bacteriol. 2007, 189:3228-3236.
42. Jores J., Rumer L., Wieler L. Impact of the locus of enterocyte effacement pathogenicity island on the evolution of pathogenic Escherichia coli. Int. J. Med. Microbiol. 2004, 294:102-113.
43. Karaolis D.K., Johnson J.A., Bailey C.C., Boedeker E.C., Kaper J.B., Reeves P.R. A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:3134-3139.
44. Karlin S. Detecting anomalous gene clusters and pathogenicity islands in diverse bacterial genomes. Trends Microbiol. 2001, 9:335-343.
45. Klockgether J., Reva O., Larbig K., Tummler B. Sequence analysis of the mobile genome island pKLC102 of Pseudomonas aeruginosa C. J. Bacteriol. 2004, 186:518-534.
46. Klockgether J., Wurdemann D., Reva O., Wiehlmann L., Tummler B. Diversity of the abundant pKLC102/PAGI-2 family of genomic islands in Pseudomonas aeruginosa. J. Bacteriol. 2007, 189:2443-2459.
47. Larkin M.A., Blackshields G., Brown N.P., et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
48. Lavigne J., Blanc-Potard A. Molecular evolution of Salmonella enterica serovar Typhimurium and pathogenic Escherichia coli: from pathogenesis to therapeutics. Infect. Genet. Evol. 2008, 8:217-226.
49. Leopold S., Shaikh N., Tarr P. Further evidence of constrained radiation in the evolution of pathogenic Escherichia coli O157:H7. Infect. Genet. Evol. 2010, (Epub ahead of print).
50. Leplae R., Lima-Mendez G., Toussaint A. ACLAME: a CLAssification of Mobile genetic Elements. Nucleic Acids Res. 2010, 38:D57-61.
51. Lesic B., Bach S., Ghigo J.M., Dobrindt U., Hacker J., Carniel E. Excision of the high-pathogenicity island of Yersinia pseudotuberculosis requires the combined actions of its cognate integrase and Hef, a new recombination directionality factor. Mol. Microbiol. 2004, 52:1337-1348.
52. Lewis J.A., Hatfull G.F. Control of directionality in integrase-mediated recombination: examination of recombination directionality factors (RDFs) including Xis and Cox proteins. Nucleic Acids Res. 2001, 29:2205-2216.
53. Lima-Mendez G., Toussaint A., Leplae R. Analysis of the phage sequence space: the benefit of structured information. Virology 2007, 365:241-249.
54. Lima-Mendez G., Van Helden J., Toussaint A., Leplae R. Prophinder: a computational tool for prophage prediction in prokaryotic genomes. Bioinformatics 2008, 24:863-865.
55. Luck S.N., Turner S.A., Rajakumar K., Sakellaris H., Adler B. Ferric dicitrate transport system (Fec) of Shigella flexneri 2a YSH6000 is encoded on a novel pathogenicity island carrying multiple antibiotic resistance genes. Infect. Immun. 2001, 69:6012-6021.
56. Luck S.N., Turner S.A., Rajakumar K., Adler B., Sakellaris H. Excision of the Shigella resistance locus pathogenicity island in Shigella flexneri is stimulated by a member of a new subgroup of recombination directionality factors. J. Bacteriol. 2004, 186:5551-5554.
57. Martinez-Guerrero C.E., Ciria R., Abreu-Goodger C., Moreno-Hagelsieb G., Merino E. GeConT 2: gene context analysis for orthologous proteins, conserved domains and metabolic pathways. Nucleic Acids Res. 2008, 36:W176-W180.
58. Mazel D. Integrons: agents of bacterial evolution. Nat. Rev. Microbiol. 2006, 4:608-620.
59. Mellmann A., Fruth A., Friedrich A., Wieler L., Harmsen D., Werber D., Middendorf B., Bielaszewska M., Karch H. Phylogeny and disease association of Shiga toxin-producing Escherichia coli O91. Emerg. Infect. Dis. 2009, 15:1474-1477.
60. Messier N., Roy P.H. Integron integrases possess a unique additional domain necessary for activity. J. Bacteriol. 2001, 183:6699-6706.
61. Middendorf B., Hochhut B., Leipold K., Dobrindt U., Blum-Oehler G., Hacker J. Instability of pathogenicity islands in uropathogenic Escherichia coli 536. J. Bacteriol. 2004, 186:3086-3096.
62. Milne I., Wright F., Rowe G., Marshall D.F., Husmeier D., McGuire G. TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments. Bioinformatics 2004, 20:1806-1807.
63. Mohd-Zain Z., Turner S.L., Cerdeno-Tarraga A.M., et al. Transferable antibiotic resistance elements in Haemophilus influenzae share a common evolutionary origin with a diverse family of syntenic genomic islands. J. Bacteriol. 2004, 186:8114-8122.
64. Murphy D., Pembroke J. Transfer of the IncJ plasmid R391 to recombination deficient Escherichia coli K12: evidence that R391 behaves as a conjugal transposon. FEMS Microbiol. Lett. 1995, 134:153-158.
65. Murphy R.A., Boyd E.F. Three pathogenicity islands of Vibrio cholerae can excise from the chromosome and form circular intermediates. J. Bacteriol. 2008, 190:636-647.
66. Nemergut D.R., Robeson M.S., Kysela R.F., Martin A.P., Schmidt S.K., Knight R. Insights and inferences about integron evolution from genomic data. BMC Genomics 2008, 9:261.
67. Nicholas K.B., Deerfield D.W. Genedoc: analysis and visualization of genetic variation. EMBNEW 1997.
68. Nugent M. A conjugative 'plasmid' lacking autonomous replication. J. Gen. Microbiol. 1981, 126:305-310.
69. Nunes-Duby S.E., Kwon H.J., Tirumalai R.S., Ellenberger T., Landy A. Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res. 1998, 26:391-406.
70. Ochman H., Whittam T.S., Caugant D.A., Selander R.K. Enzyme polymorphism and genetic population structure in Escherichia coli and Shigella. J. Gen. Microbiol. 1983, 129:2715-2726.
71. Ochman H., Selander R.K. Evidence for clonal population structure in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 1984, 81:198-201.
72. Ochman H., Selander R.K. Standard reference strains of Escherichia coli from natural populations. J. Bacteriol. 1984, 157:690-693.
73. Ochman H., Jones I.B. Evolutionary dynamics of full genome content in Escherichia coli. EMBO J. 2000, 19:6637-6643.
74. Osborn A.M., Boltner D. When phage, plasmids, and transposons collide: genomic islands, and conjugative- and mobilizable-transposons as a mosaic continuum. Plasmid 2002, 48:202-212.
75. Pembroke J., MacMahon C., McGrath B. The role of conjugative transposons in the Enterobacteriaceae. Cell. Mol. Life Sci. 2002, 59:2055-2064.
76. Perna N.T., Plunkett G., Burland V., et al. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 2001, 409:529-533.
77. Quirke A.M., Reen F.J., Claesson M.J., Boyd E.F. Genomic island identification in Vibrio vulnificus reveals significant genome plasticity in this human pathogen. Bioinformatics 2006, 22:905-910.
78. Rajakumar K., Sasakawa C., Adler B. Use of a novel approach, termed island probing, identifies the Shigella flexneri she pathogenicity island which encodes a homolog of the immunoglobulin A protease-like family of proteins. Infect. Immun. 1997, 65:4606-4614.
79. Rajanna C., Wang J., Zhang D., Xu Z., Ali A., Hou Y.M., Karaolis D.K. The vibrio pathogenicity island of epidemic Vibrio cholerae forms precise extrachromosomal circular excision products. J. Bacteriol. 2003, 185:6893-6901.
80. Recchia G.D., Hall R.M. Origins of the mobile gene cassettes found in integrons. Trends Microbiol. 1997, 5:389-394.
81. Roberts A., Chandler M., Courvalin P., et al. Revised nomenclature for transposable genetic elements. Plasmid 2008, 60:167-173.
82. Ronquist F., Huelsenbeck J. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
83. Salyers A.A., Whittle G., Shoemaker N.B. Conjugative and mobilizable transposons. Microbial Evolution Gene Establishment, Survival, and Exchange 2004, 125-157. ASM Press, Washington, DC. R.V. Miller, M.J. Day (Eds.).
84. Schubert S., Darlu P., Clermont O., et al. Role of intraspecies recombination in the spread of pathogenicity islands within the Escherichia coli species. PLoS Pathog. 2009, 5:e1000257. (Epub).
85. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
86. Tenaillon O., Skurnik D., Picard B., Denamur E. The population genetics of commensal Escherichia coli. Nat. Rev. Microbiol. 2010, 8:207-211.
87. Touchon M., Hoede C., Tenaillon O., et al. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 2009, 5:e1000344.
88. Toussaint A., Merlin C. Mobile elements as a combination of functional modules. Plasmid 2002, 47:26-35.
89. Toussaint A., Lima-Mendez G., Leplae R. PhiGO, a phage ontology associated with the ACLAME database. Res. Microbiol. 2007, 158:567-571.
90. van Passel M.W., Luyf A.C., van Kampen A.H., Bart A., van der Ende A. Deltarho-web, an online tool to assess composition similarity of individual nucleic acid sequences. Bioinformatics 2005, 21:3053-3055.
91. Waldor M.K., Tschape H., Mekalanos J.J. A new type of conjugative transposon encodes resistance to sulfamethoxazole, trimethoprim, and streptomycin in Vibrio cholerae O139. J. Bacteriol. 1996, 178:4157-4165.
92. Welch R.A., Burland V., Plunkett G., et al. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:17020-17024.
93. Whittam T.S., Ochman H., Selander R.K. Geographic components of linkage disequilibrium in natural populations of Escherichia coli. Mol. Biol. Evol. 1983, 1:67-83.
94. Whittam T.S., Ochman H., Selander R.K. Multilocus genetic structure in natural populations of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 1983, 80:1751-1755.
95. Whittle G., Shoemaker N.B., Salyers A.A. The role of Bacteroides conjugative transposons in the dissemination of antibiotic resistance genes. Cell. Mol. Life Sci. 2002, 59:2044-2054.
96. Wilde C., Mazel D., Hochhut B., Middendorf B., Le Roux F., Carniel E., Dobrindt U., Hacker J. Delineation of the recombination sites necessary for integration of pathogenicity islands II and III into the Escherichia coli 536 chromosome. Mol. Microbiol. 2008, 68:139-151.